The duration of intrauterine development influences discrimination of speech prosody in infants.
fNIRS
functional imaging
language development
preterm birth
speech discrimination
Journal
Developmental science
ISSN: 1467-7687
Titre abrégé: Dev Sci
Pays: England
ID NLM: 9814574
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
revised:
17
02
2021
received:
28
08
2020
accepted:
05
03
2021
pubmed:
6
4
2021
medline:
21
10
2021
entrez:
5
4
2021
Statut:
ppublish
Résumé
Auditory speech discrimination is essential for normal language development. Children born preterm are at greater risk of language developmental delays. Using functional near-infrared spectroscopy at term-equivalent age, the present study investigated early discrimination of speech prosody in 62 neonates born between week 23 and 41 of gestational age (GA). We found a significant positive correlation between GA at birth and neural discrimination of forward versus backward speech at term-equivalent age. Cluster analysis identified a critical threshold at around week 32 of GA, pointing out the existence of subgroups. Infants born before week 32 of GA exhibited a significantly different pattern of hemodynamic response to speech stimuli compared to infants born at or after week 32 of GA. Thus, children born before the GA of 32 weeks are especially vulnerable to early speech discrimination deficits. To support their early language development, we therefore suggest a close follow-up and additional speech and language therapy especially in the group of children born before week 32 of GA.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13110Subventions
Organisme : Austrian Science Fund FWF
ID : KLI 544
Pays : Austria
Informations de copyright
© 2021 The Authors. Developmental Science published by John Wiley & Sons Ltd.
Références
Allotey, J., Zamora, J., Cheong-See, F., Kalidindi, M., Arroyo-Manzano, D., Asztalos, E., van der Post, J. A. M, Mol, B. W., Moore, D., Birtles, D., Khan, K. S., & Thangaratinam, S. (2017). Cognitive, motor, behavioural and academic performances of children born preterm: a meta-analysis and systematic review involving 64 061 children. BJOG: An International Journal of Obstetrics and Gynecology, 125(1), 16-25. https://doi.org/10.1111/1471-0528.14832
Arimitsu, T., Minagawa, Y., Yagihashi, T., Uchida, M. O., Matsuzaki, A., Ikeda, K., & Takahashi, T. (2018). The cerebral hemodynamic response to phonetic changes of speech in preterm and term infants: The impact of postmenstrual age. NeuroImage: Clinical, 19, 599-606. https://doi.org/10.1016/j.nicl.2018.05.005
Arpino, C., Compagnone, E., Montanaro, M. L., Cacciatore, D., De Luca, A., Cerulli, A., Di Girolamo, S., & Curatolo, P. (2010). Preterm birth and neurodevelopmental outcome: A review. Childs Nervous System, 26(9), 1139-1149. https://doi.org/10.1007/s00381-010-1125-y
Barre, N., Morgan, A., Doyle, L. W., & Anderson, P. J. (2011). Language abilities in children who were very preterm and/or very low birth weight: A meta-analysis. Journal of Pediatrics, 158(5), 766-774.e1. https://doi.org/10.1016/j.jpeds.2010.10.032
Bartha-Doering, L., Alexopoulos, J., Giordano, V., Stelzer, L., Kainz, T., Benavides-Varela, S., Wartenburger, I., Klebermass-Schrehof, K., Olischar, M., Seidl, R., & Berger, A. (2019). Absence of neural speech discrimination in preterm infants at term-equivalent age. Developmental Cognitive Neuroscience, 39, 100679. https://doi.org/10.1016/j.dcn.2019.100679
Bartha-Doering, L., Deuster, D., Giordano, V., am Zehnhoff-Dinnesen, A., & Dobel, C. (2015). A systematic review of the mismatch negativity as an index for auditory sensory memory: From basic research to clinical and developmental perspectives. Psychophysiology, 52(9), 1115-1130. https://doi.org/10.1111/psyp.12459
Benasich, A. A., & Tallal, P. (2002). Infant discrimination of rapid auditory cues predicts later language impairment. Behavioural Brain Research, 136(1), 31-49.Retrieved from https://doi.org/10.1016/S0166-4328(02)00098-0
Benavides-Varela, S., & Gervain, J. (2017). Learning word order at birth: A NIRS study. Developmental Cognitive Neuroscience, 25, 198-208. https://doi.org/10.1016/j.dcn.2017.03.003
Benavides-Varela, S., Hochmann, J. R., Macagno, F., Nespor, M., & Mehler, J. (2012). Newborn's brain activity signals the origin of word memories. Proceedings of the National Academy of Sciences of the United States of America, 109(44), 17908-17913. https://doi.org/10.1073/pnas.1205413109
Bertsch, M., Reuter, M., Czedik-Eysenberg, I., Berger, A., Olischar, M., Bartha-Doering, L., & Giordano, V. (2020). The “Sound of Silence” in a neonatal intensive care unit - Listening to speech and music inside an incubator. Frontiers in Psychology, 11, 1055. https://doi.org/10.3389/fpsyg.2020.01055
Chang, E. F., & Merzenich, M. M. (2003). Environmental noise retards auditory cortical development. Science, 300(5618), 498-502. https://doi.org/10.1126/science.1082163
Coenraad, S., Goedegebure, A., & Hoeve, L. J. (2011). An initial overestimation of sensorineural hearing loss in NICU infants after failure on neonatal hearing screening. International Journal of Pediatric Otorhinolaryngology, 75(2), 159-162. https://doi.org/10.1016/j.ijporl.2010.10.026
Colella-Santos, M. F., Hein, T. A., de Souza, G. L., do Amaral, M. I., & Casali, R. L. (2014). Newborn hearing screening and early diagnostic in the NICU. BioMed Research International, 2014, 845308. https://doi.org/10.1155/2014/845308
Cristia, A., & Seidl, A. (2011). Sensitivity to prosody at 6 months predicts vocabulary at 24 months. In N. Danis, K. Mesh, & H. Sung (Eds.), BUCLD 35: Proceedings of the 35th annual Boston University Conference on Language Development (pp. 145-156). Somerville, Mass: Cascadilla Press.
Davidesko, S., Pariente, G., Wainstock, T., & Sheiner, E. (2020). 672: Is there a critical threshold? Preterm delivery and long term infectious morbidity of the offspring. American Journal of Obstetrics & Gynecology, 222(1), S427-S428. https://doi.org/10.1016/j.ajog.2019.11.687
DeCasper, A., & Fifer, W. (1980). Of human bonding: Newborns prefer their mothers' voice. Science (New York, N.Y.), 208, 1174-1176. https://doi.org/10.1126/science.7375928
Decasper, A., Lecanuet, J., Busnel, M., & Granier-Deferre, C. (1994). Fetal reaction to recurrent maternal speech. Infant Behavior & Development, 17, 159-164. https://doi.org/10.1016/0163-6383(94)90051-5
DeCasper, A., & Spence, M. J. (1986). Prenatal maternal speech influences newborns' perception of speech sounds. Infant Behavior and Development, 9(2), 133-150. https://doi.org/10.1016/0163-6383(86)90025-1
Dehaene-Lambertz, G., Dehaene, S., & Hertz-Pannier, L. (2002). Functional neuroimaging of speech perception in infants. Science, 298(5600), 2013-2015. https://doi.org/10.1126/science.1077066
du Plessis, A. J. (2009). The role of systemic hemodynamic disturbances in prematurity-related brain injury. Journal of Child Neurology, 24(9), 1127-1140. https://doi.org/10.1177/0883073809339361
Fiori, S., & Guzzetta, A. (2015). Plasticity following early-life brain injury: Insights from quantitative MRI. Seminars in Perinatology, 39(2), 141-146. https://doi.org/10.1053/j.semperi.2015.01.007
Gerhardt, K. J., & Abrams, R. M. (2000). Fetal exposures to sound and vibroacoustic stimulation. Journal of Perinatology, 20(8 Pt 2), S21-S30. https://doi.org/10.1038/sj.jp.7200446
Gervain, J., Mehler, J., Werker, J. F., Nelson, C. A., Csibra, G., Lloyd-Fox, S., Shukla, M., & Aslin, R. N. (2011). Near-infrared spectroscopy: A report from the McDonnell infant methodology consortium. Developmental Cognitive Neuroscience, 1(1), 22-46. https://doi.org/10.1016/j.dcn.2010.07.004
Goswami, U. (2019). Speech rhythm and language acquisition: An amplitude modulation phase hierarchy perspective. Annals of the New York Academy of Sciences, 1453, 67-78. https://doi.org/10.1111/nyas.14137
Graven, S. N., & Browne, J. V. (2008). Auditory development in the fetus and infant. Newborn and Infant Nursing Reviews, 8(4), 187-193. https://doi.org/10.1053/j.nainr.2008.10.010
Guarini, A., Marini, A., Savini, S., Alessandroni, R., Faldella, G., & Sansavini, A. (2016). Linguistic features in children born very preterm at preschool age. Developmental Medicine and Child Neurology, 58(9), 949-956. https://doi.org/10.1111/dmcn.13118
Guarini, A., Sansavini, A., Fabbri, C., Alessandroni, R., Faldella, G., & Karmiloff-Smith, A. (2009). Reconsidering the impact of preterm birth on language outcome. Early Human Development, 85(10), 639-645. https://doi.org/10.1016/j.earlhumdev.2009.08.061
Guarini, A., Sansavini, A., Fabbri, C., Savini, S., Alessandroni, R., Faldella, G., & Karmiloff-Smith, A. (2010). Long-term effects of preterm birth on language and literacy at eight years. Journal of Child Language, 37(4), 865-885. https://doi.org/10.1017/S0305000909990109
Guzzetta, F., Conti, G., & Mercuri, E. (2011). Auditory processing in infancy: Do early abnormalities predict disorders of language and cognitive development? Developmental Medicine and Child Neurology, 53(12), 1085-1090. https://doi.org/10.1111/j.1469-8749.2011.04084.x
Harshaw, C., & Lickliter, R. (2011). Biased embryos: Prenatal experience alters the postnatal malleability of auditory preferences in bobwhite quail. Developmental Psychobiology, 53, 291-302. https://doi.org/10.1002/dev.20521
Hepper, P. G. (1988). Fetal “soap” addiction. The Lancet, 331(8598), 1347-1348. https://doi.org/10.1016/S0140-6736(88)92170-8
Hepper, P. G., & Shahidullah, B. S. (1994). Development of fetal hearing. Archives of Disease in Childhood. Fetal and Neonatal Edition, 71(2), F81-F87. https://doi.org/10.1136/fn.71.2.F81
Herold, B., Hohle, B., Walch, E., Weber, T., & Obladen, M. (2008). Impaired word stress pattern discrimination in very-low-birthweight infants during the first 6 months of life. Developmental Medicine and Child Neurology, 50(9), 678-683. https://doi.org/10.1111/j.1469-8749.2008.03055.x
Huppert, T. J., Diamond, S. G., Franceschini, M. A., & Boas, D. A. (2009). HomER: A review of time-series analysis methods for near-infrared spectroscopy of the brain. Applied Optics, 48(10), D280-D298.Retrieved from https://doi.org/10.1364/AO.48.00D280
Jardri, R., Pins, D., Houfflin-Debarge, V., Chaffiotte, C., Rocourt, N., Pruvo, J. P., Steinling, M., Delion, P., & Thomas, P. (2008). Fetal cortical activation to sound at 33 weeks of gestation: A functional MRI study. Neuroimage, 42(1), 10-18. https://doi.org/10.1016/j.neuroimage.2008.04.247
Kang, M. Y., Jeong, S. W., & Kim, L. S. (2012). Changes in the hearing thresholds of infants who failed the newborn hearing screening test and in infants treated in the neonatal intensive care unit. Clinical and Experimental Otorhinolaryngology, 5(Suppl 1), S32-S36. https://doi.org/10.3342/ceo.2012.5.S1.S32
Kiserud, T., Piaggio, G., Carroli, G., Widmer, M., Carvalho, J., Neerup Jensen, L., Giordano, D., Guilherme Cecatti, J., Abdel Aleem, H., Talegawkar, S. A., Benachi, A., Diemert, A., Tshefu Kitoto, A., Thinkhamrop, J., Lumbiganon, P., Tabor, A., Kriplani, A., Gonzalez Perez, R., Hecher, K., … Platt, L. D. (2017). The World Health Organization fetal growth charts: A multinational longitudinal study of ultrasound biometric measurements and estimated fetal weight. PLoS Medicine, 14(1), e1002220. https://doi.org/10.1371/journal.pmed.1002220
Kuhl, P., & Rivera-Gaxiola, M. (2008). Neural substrates of language acquisition. Annual Review of Neuroscience, 31, 511-534. https://doi.org/10.1146/annurev.neuro.30.051606.094321
Kujala, A., Huotilainen, M., Hotakainen, M., Lennes, M., Parkkonen, L., Fellman, V., & Naatanen, R. (2004). Speech-sound discrimination in neonates as measured with MEG. Neuroreport, 15(13), 2089-2092.Retrieved from https://doi.org/10.1097/00001756-200409150-00018
Lim, R., & Brichta, A. M. (2016). Anatomical and physiological development of the human inner ear. Hearing Research, 338, 9-21. https://doi.org/10.1016/j.heares.2016.02.004
Lloyd-Fox, S., Blasi, A., & Elwell, C. E. (2010). Illuminating the developing brain: The past, present and future of functional near infrared spectroscopy. Neuroscience and Biobehavioral Reviews, 34(3), 269-284. https://doi.org/10.1016/j.neubiorev.2009.07.008
Lobe, M., & Weigel, S. (1972). Das kleine Ich bin Ich. Wien, München: Verlag Jungbrunnen.
Mahmoudzadeh, M., Dehaene-Lambertz, G., Fournier, M., Kongolo, G., Goudjil, S., Dubois, J., Grebe, R., & Wallois, F. (2013). Syllabic discrimination in premature human infants prior to complete formation of cortical layers. Proceedings of the National Academy of Sciences of the United States of America, 110(12), 4846-4851. https://doi.org/10.1073/pnas.1212220110
Mampe, B., Friederici, A., Christophe, A., & Wermke, K. (2009). Newborns' cry melody is shaped by their native language. Current Biology: CB, 19, 1994-1997. https://doi.org/10.1016/j.cub.2009.09.064
Martinez-Biarge, M., Diez-Sebastian, J., Rutherford, M. A., & Cowan, F. M. (2010). Outcomes after central grey matter injury in term perinatal hypoxic-ischaemic encephalopathy. Early Human Development, 86(11), 675-682. https://doi.org/10.1016/j.earlhumdev.2010.08.013
McMahon, E., Wintermark, P., & Lahav, A. (2012). Auditory brain development in premature infants: The importance of early experience. Annals of the New York Academy of Sciences, 1252, 17-24. https://doi.org/10.1111/j.1749-6632.2012.06445.x
Mejdoubi, M., Dedouit, F., Mokrane, F. Z., & Telmon, N. (2016). CT scan imaging of the human fetal labyrinth: Case series data throughout gestation. Otology and Neurotology, 37(5), 602-607. https://doi.org/10.1097/MAO.0000000000001039
Monson, B., Eaton-Rosen, Z., Kapur, K., Liebenthal, E., Brownell, A., Smyser, C., Rogers, C. E., Inder, T. E., Warfield, S. K., & Neil, J. (2018). Differential rates of perinatal maturation of human primary and nonprimary auditory cortex. eNeuro, 5, ENEURO.0380-0317.2017. https://doi.org/10.1523/ENEURO.0380-17.2017
Moon, C., Cooper, R. P., & Fifer, W. P. (1993). Two-day-olds prefer their native language. Infant Behavior and Development, 16(4), 495-500. https://doi.org/10.1016/0163-6383(93)80007-U
Morlet, T., Lapillonne, A., Ferber, C., Duclaux, R., Sann, L., Putet, G., Salle, B., & Collet, L. (1995). Spontaneous otoacoustic emissions in preterm neonates: Prevalence and gender effects. Hearing Research, 90(1), 44-54. https://doi.org/10.1016/0378-5955(95)00144-4
Morokuma, S., Fukushima, K., Kawai, N., Tomonaga, M., Satoh, S., & Nakano, H. (2004). Fetal habituation correlates with functional brain development. Behavioural Brain Research, 153(2), 459-463. https://doi.org/10.1016/j.bbr.2004.01.002
Naoi, N., Fuchino, Y., Shibata, M., Niwa, F., Kawai, M., Konishi, Y., Okanoya, K., & Myowa-Yamakoshi, M. (2013). Decreased right temporal activation and increased interhemispheric connectivity in response to speech in preterm infants at term-equivalent age. Frontiers in Psychology, 4, 94. https://doi.org/10.3389/fpsyg.2013.00094
Nazzi, T., Bertoncini, J., & Mehler, J. (1998). Language discrimination by newborns: Toward an understanding of the role of rhythm. Journal of Experimental Psychology. Human Perception and Performance, 24(3), 756-766.Retrieved from https://doi.org/10.1037/0096-1523.24.3.756
Nourhashemi, M., Mahmoudzadeh, M., Goudjil, S., Kongolo, G., & Wallois, F. (2019). Neurovascular coupling in the developing neonatal brain at rest. Human Brain Mapping, 41, 503-519. https://doi.org/10.1002/hbm.24818
Partanen, E., Kujala, T., Tervaniemi, M., & Huotilainen, M. (2013). Prenatal music exposure induces long-term neural effects. PLoS One, 8(10), e78946. https://doi.org/10.1371/journal.pone.0078946
Pasman, R. L., Näätänen, R., & Alho, K. (1991). Auditory evoked responses in prematures. Infant Behaviour and Development, 14, 129-135.
Peña, M., Maki, A., Kovačić, D., Dehaene-Lambertz, G., Koizumit, H., Bouquet, F., & Mehler, J. (2003). Sounds and silence: An optical topography study of language recognition at birth. Proceedings of the National Academy of Sciences of the United States of America, 100(20), 11702-11705. https://doi.org/10.1073/pnas.1934290100
Peña, M., Pittaluga, E., & Farkas, C. (2010). [Phonological acquisition in preterm infants]. Revista De Neurologia, 50(1), 12-18.Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/20073018
Peña, M., Pittaluga, E., & Mehler, J. (2010). Language acquisition in premature and full-term infants. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 3823-3828. https://doi.org/10.1073/pnas.0914326107
Prieto, P., & Esteve-Gibert, N. (2018). The development of prosody in first language acquisition. Amsterdam: John Benjamins.
Ramus, F., Hauser, M. D., Miller, C., Morris, D., & Mehler, J. (2000). Language discrimination by human newborns and by cotton-top tamarin monkeys. Science, 288(5464), 349-351. https://doi.org/10.1126/science.288.5464.349
Ramus, F., Nespor, M., & Mehler, J. (1999). Correlates of linguistic rhythm in the speech signal. Cognition, 73(3), 265-292.Retrieved from https://doi.org/10.1016/S0010-0277(99)00058-X
Saffran, J. R., & Thiessen, E. D. (2003). Pattern induction by infant language learners. Developmental Psychology, 39(3), 484-494. https://doi.org/10.1037/0012-1649.39.3.484
Sassenhagen, J., & Draschkow, D. (2019). Cluster-based permutation tests of MEG/EEG data do not establish significance of effect latency or location. Psychophysiology, 56(6), e13335. https://doi.org/10.1111/psyp.13335
Sato, H., Hirabayashi, Y., Tsubokura, H., Kanai, M., Ashida, T., Konishi, I., Uchida-Ota, M., Konishi, Y., & Maki, A. (2012). Cerebral hemodynamics in newborn infants exposed to speech sounds: A whole-head optical topography study. Human Brain Mapping, 33(9), 2092-2103. https://doi.org/10.1002/hbm.21350
Schaadt, G., Mannel, C., van der Meer, E., Pannekamp, A., Oberecker, R., & Friederici, A. D. (2015). Present and past: Can writing abilities in school children be associated with their auditory discrimination capacities in infancy? Research in Developmental Disabilities, 47, 318-333. https://doi.org/10.1016/j.ridd.2015.10.002
Speer, S., & Ito, K. (2009). Prosody in first language acquisition - Acquiring intonation as a tool to organize information in conversation. Language and Linguistics Compass, 31(1), 90-110. https://doi.org/10.1111/j.1749-818X.2008.00103.x
Taylor, C. L., Christensen, D., Lawrence, D., Mitrou, F., & Zubrick, S. R. (2013). Risk factors for children's receptive vocabulary development from four to eight years in the longitudinal study of Australian children. PLoS One, 8(9), e73046. https://doi.org/10.1371/journal.pone.0073046
Twilhaar, E. S., de Kieviet, J. F., Aarnoudse-Moens, C. S., van Elburg, R. M., & Oosterlaan, J. (2018). Academic performance of children born preterm: a meta-analysis and meta-regression. Archives of Disease in Childhood. Fetal and Neonatal Edition, 103(4), F322-F330. https://doi.org/10.1136/archdischild-2017-312916
van Noort-van der Spek, I. L., Franken, M. C., & Weisglas-Kuperus, N. (2012). Language functions in preterm-born children: A systematic review and meta-analysis. Pediatrics, 129(4), 745-754. https://doi.org/10.1542/peds.2011-1728
van Zuijen, T. L., Plakas, A., Maassen, B. A., Maurits, N. M., & van der Leij, A. (2013). Infant ERPs separate children at risk of dyslexia who become good readers from those who become poor readers. Developmental Science, 16(4), 554-563. https://doi.org/10.1111/desc.12049
Vohr, B. (2014). Speech and language outcomes of very preterm infants. Seminars in Fetal & Neonatal Medicine, 19(2), 78-83. https://doi.org/10.1016/j.siny.2013.10.007
Webb, A. R., Heller, H. T., Benson, C. B., & Lahav, A. (2015). Mother's voice and heartbeat sounds elicit auditory plasticity in the human brain before full gestation. Proceedings of the National Academy of Sciences, 112(10), 3152-3157. https://doi.org/10.1073/pnas.1414924112
Weber, C., Hahne, A., Friedrich, M., & Friederici, A. (2004). Discrimination of word stress in early infant perception: Electrophysiological evidence. Brain Research. Cognitive Brain Research, 18, 149-161. https://doi.org/10.1016/j.cogbrainres.2003.10.001
WHO. (2020). Preterm birth. Retrieved from https://www.who.int/news-room/fact-sheets/detail/preterm-birth
Wolke, D., Samara, M., Bracewell, M., Marlow, N., & Group, E. P. S. (2008). Specific language difficulties and school achievement in children born at 25 weeks of gestation or less. Journal of Pediatrics, 152(2), 256-262. https://doi.org/10.1016/j.jpeds.2007.06.043
Wu, D., Chang, L., Akazawa, K., Oishi, K., Skranes, J., Ernst, T., & Oishi, K. (2017). Mapping the critical gestational age at birth that alters brain development in preterm-born infants using multi-modal MRI. Neuroimage, 149, 33-43. https://doi.org/10.1016/j.neuroimage.2017.01.046
Yucel, M., Selb, J., Cooper, R., & Boas, D. (2014). Targeted principle component analysis: A new motion artifact correction approach for near-infrared spectroscopy. Journal of Innovative Optical Health Sciences, 07, 1350066. https://doi.org/10.1142/S1793545813500661